Experimental and Applied Acarology

, Volume 67, Issue 1, pp 21–34 | Cite as

Phytoseiids in Washington commercial apple orchards: biodiversity and factors affecting abundance

  • Rebecca A. Schmidt-Jeffris
  • Elizabeth H. Beers
  • David W. Crowder
Article

Abstract

Galendromus occidentalis (Nesbitt) is an important biological control agent of spider mites (Acari: Tetranychidae) in Washington apple orchards. It was thought to be essentially the sole phytoseiid existing in this system, due in part to its resistance to commonly used orchard pesticides, and organophosphates in particular. To test this assumption, we conducted a survey of 102 commercial apple blocks in Washington to characterize the community of phytoseiid species. Seven phytoseiid species were found in our samples; G. occidentalis and Amblydromella caudiglans (Schuster) were found in the greatest abundance. We hypothesized that the gradual shift away from the use of organophosphates in recent decades may have caused the change in phytoseiid community structure. The survey data and information regarding the management, location, and surrounding habitat of each block were used to determine what factors affect phytoseiid abundances. Galendromus occidentalis abundance was positively affected by the use of conventional (vs. organic) spray programs, and the use of the acaricide bifenazate. Amblydromella caudiglans abundance was negatively affected by bifenazate use and positively affected by herbicide strip weediness; it was also less prevalent in ‘Golden Delicious’ blocks compared to other cultivars. These results indicate that A. caudiglans reaches higher abundances in orchards that lack certain agricultural disturbances, whereas G. occidentalis can survive in more disturbed environments. Surveys of this nature can provide valuable insight to potential drivers of community structure, allowing for the improvement of integrated pest management programs that incorporate conservation of newly recognized biological control agents such as A. caudiglans.

Keywords

Phytoseiidae Galendromus occidentalis Amblydromella caudiglans Landscape ecology Biodiversity Apple 

Supplementary material

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References

  1. Abad-Moyano R, Urbaneja A, Hoffmann D, Schausberger P (2010) Effect of Euseius stipulatus on establishment and efficacy in spider mite suppression of Neoseiulus californicus and Phytoseiulus persimilis in clementine. Exp Appl Acarol 50:329–341PubMedCrossRefGoogle Scholar
  2. Aguilar-Fenollosa E, Ibanez-Gual MV, Pascual-Ruiz S, Hurtado M, Jacas JA (2011) Effect of ground-cover management on spider mites and their phytoseiid natural enemies in clementine mandarin orchards (II): top–down regulation mechanisms. Biol Control 59:171–179CrossRefGoogle Scholar
  3. Alston DG (1994) Effect of apple orchard floor vegetation on density and dispersal of phytophagous and predaceous mites in Utah. Agric Ecosyst Environ 50:73–84CrossRefGoogle Scholar
  4. Barber A, Campbell CAM, Crane H, Lilley R, Tregidga E (2003) Biocontrol of two-spotted spider mite Tetranychus urticae on dwarf hops by the phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus. Biocontrol Sci. Technol. 13:275–284CrossRefGoogle Scholar
  5. Beers EH, Schmidt RA (2014) Impacts of orchard pesticides on Galendromus occidentalis: lethal and sublethal effects. Crop Prot 56:16–24CrossRefGoogle Scholar
  6. Beers EH, Brunner JF, Dunley JE, Doerr M, Granger K (2005) Role of neonicotinyl insecticides in Washington apple integrated pest management. Part II. Nontarget effects on integrated mite control. J Insect Sci 5(16):1–10Google Scholar
  7. Berkett LP, Forsythe HY (1980) Predaceous mites (Acari) associated with apple foliage in Maine. Can Entomol 112:497–502CrossRefGoogle Scholar
  8. Bostanian NJ, Hardman JM, Racette G, Franklin J, Lasnier J (2006) Inventory of predacious mites in Quebec commercial apple orchards where integrated pest management programs are implemented. Ann Entomol Soc Am 99:536–544CrossRefGoogle Scholar
  9. Bostanian NJ, Thistlewood HA, Hardman JM, Laurin M-C, Racette G (2009) Effect of seven new orchard pesticides on Galendromus occidentalis in laboratory studies. Pest Manag Sci 65:635–639PubMedCrossRefGoogle Scholar
  10. Bostanian NJ, Hardman JM, Thistlewood HA, Racette G (2010) Effects of six selected orchard insecticides on Neoseiulus fallacis. Pest Manag Sci 66:1263–1267PubMedCrossRefGoogle Scholar
  11. Clements DR, Harmsen R (1990) Predatory behavior and prey-stage preferences of stigmaeid and phytoseiid mites and their potential compatibility in biological control. Can Entomol 122:321–328CrossRefGoogle Scholar
  12. Croft BA (1982) Apple pest management. In: Metcalf RL, Luckmann WH (eds) Introduction to insect pest management. Wiley-Interscience, New York, pp 465–498Google Scholar
  13. Croft BA (1990) Endemic species. In: Arthropod biological control agents and pesticides. Wiley, New York, pp 431–453Google Scholar
  14. Croft BA, Luh H-K (2004) Phytoseiid mites on unsprayed apple trees in Oregon, and other western states (USA): distributions, life-style types and relevance to commercial orchards. Exp Appl Acarol 33:281–326PubMedCrossRefGoogle Scholar
  15. Croft BA, MacRae IV (1992a) Biological control of apple mites by mixed populations of Metaseiulus occidentalis (Nesbitt) and Typhlodromus pyri Scheuten (Acari: Phytoseiidae). Environ Entomol 21:202–209CrossRefGoogle Scholar
  16. Croft BA, MacRae IV (1992b) Persistence of Typhlodromus pyri and Metaseiulus occidentalis (Acari: Phytoseiidae) on apple after inoculative release and competition with Zetzellia mali (Acari: Stigmaeidae). Environ Entomol 21:1168–1177CrossRefGoogle Scholar
  17. Croft BA, MacRae IV (1993) Biological control of apple mites: impact of Zetzellia mali (Acari: Stigmaeidae) on Typhlodromus pyri and Metaseiulus occidentalis (Acari: Phytoseiidae). Environ Entomol 22:865–873CrossRefGoogle Scholar
  18. Croft BA, McGroarty DL (1977) The role of Amblyseius fallacis (Acarina: Phytoseiidae) in Michigan apple orchards. Farm Sci 333:2–22Google Scholar
  19. Denmark HA, Evans GA (2011) Phytoseiidae of North America and Hawaii (Acari: Mesostigmata). Indira Publishing House, West Bloomfield, MIGoogle Scholar
  20. Downing RS, Moilliet TK (1967) Relative densities of predaceous and phytophagous mites on three varieties of apple trees. Can Entomol 99:738–741CrossRefGoogle Scholar
  21. Downing RS, Moilliet TK (1972) Replacement of Typhlodromus occidentalis by T. caudiglans and T. pyri (Acarina: Phytoseiidae) after cessation of sprays on apple trees. Can Entomol 104:937–940CrossRefGoogle Scholar
  22. Duso C, Fanti M, Pozzebon A, Angeli G (2009) Is the predatory mite Kampimodromus aberrans a candidate for the control of phytophagous mites in European apple orchards? Biocontrol 54:369–382CrossRefGoogle Scholar
  23. Duso C, Ahmad S, Tirello P, Pozzebon A, Klaric V, Baldessari M, Malagnini V, Angeli G (2014) The impact of insecticides applied in apple orchards on the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae). Exp Appl Acarol 62:391–414PubMedCrossRefGoogle Scholar
  24. Environmental Protection Agency (2012) Azinphos-methyl uses cancellation 30 Sept 2012; use of existing stocks allowed through September 2013. http://www.epa.gov/oppfead1/cb/csb_page/updates/2012/azinphos-methyl.html
  25. Environmental Protection Agency (2014) Conventional reduced risk pesticide program. Pesticide registration. http://www2.epa.gov/pesticide-registration/conventional-reduced-risk-pesticide-program
  26. ESRI (2010) ArcGIS Desktop: Release 10. Redlands, CAGoogle Scholar
  27. Gadino AN, Walton VM, Dreves AJ (2011) Impact of vineyard pesticides on a beneficial arthropod, Typhlodromus pyri (Acari: Phytoseiidae), in laboratory bioassays. J Econ Entomol 104:970–977PubMedCrossRefGoogle Scholar
  28. Gerson U, Smiley RL, Ochoa R (2003) The effect of host plants and the ground cover on acarine biocontrol agents. In: Mites (Acari) for pest control. Blackwell Science, Oxford, pp 332–359Google Scholar
  29. Griffin JN, Byrnes JE, Cardinale BJ (2013) Predator richness and prey suppression: meta-analysis reveals importance of scale and phylogenetic diversity. Ecology 94:2180–2218PubMedCrossRefGoogle Scholar
  30. Horton DR, Broers DA, Hinojosa T, Lewis TM, Miliczky ER, Lewis RR (2002) Diversity and phenology of predatory arthropods overwintering in cardboard bands place in pear and apple orchards of central Washington State. Ann Entomol Soc Am 95:469–480CrossRefGoogle Scholar
  31. Hoy MA (2011) Integrated mite management in Washington apple orchards. In: Agricultural acarology: introduction to integrated mite management. Taylor and Francis Group, LLC, Boca Raton, FL, pp 237–242Google Scholar
  32. Hoyt SC (1969) Integrated chemical control of insects and biological control of mites on apple in Washington. J Econ Entomol 62:74–86CrossRefGoogle Scholar
  33. Hoyt SC (1991) Biology, ecology and control of mites in Washington orchards. In: Williams K (ed) New directions in tree fruit pest management. Good Fruit Grower, Yakima, WA, pp 147–156Google Scholar
  34. Huang M-D, Mai S-W, Li S-X, Situ J (1983) Biological control of citrus red mite, Panonychus citri (McG.) in Guangdong Province. In: Matsumoto K (ed) Proceedings, 4th international citrus congress, 9–12 Nov 1981, Tokyo, Japan. International Society of Citriculture, pp 643–646Google Scholar
  35. Jones VP, Brunner JF (1993) Degree-day models. In: Beers EH, Brunner JF, Willett MJ, Warner GM (eds) Orchard pest management: a resource book for the Pacific Northwest. Good Fruit Grower, Yakima, WAGoogle Scholar
  36. Kawashima M, Jung C (2010) Artificial ground shelters for overwintering phytoseiid mites in orchards. Exp Appl Acarol 52:35–47PubMedCrossRefGoogle Scholar
  37. Lefebvre M, Bostanian NJ, Thistlewood HMA, Mauffette Y, Racette G (2011) A laboratory assessment of the toxic attributes of six ‘reduced risk insecticides’ on Galendromus occidentalis (Acari: Phytoseiidae). Chemosphere 84:25–30PubMedCrossRefGoogle Scholar
  38. Lefebvre M, Bostanian NJ, Mauffette Y, Racette G, Thistlewood HA, Hardman JM (2012) Laboratory-based toxicological assessments of new insecticides on mortality and fecundity of Neoseiulus fallacis (Acari: Phytoseiidae). J Econ Entomol 105:866–871PubMedCrossRefGoogle Scholar
  39. Madsen HF (1964). Integrated control of phytophagous mites on apple and pear. In: Proceedings, 60th annual meeting of the Washington State Horticultural Association, 7–9 Dec 1964. Washington State Horticultural Association, Wenatchee, WA, pp 75–78Google Scholar
  40. Mailloux J, Le Bellec F, Kreiter S, Tixier M-S, Dubois P (2010) Influence of ground cover management on diversity and density of phytoseiid mites (Acari: Phytoseiidae) in Guadeloupean citrus orchards. Exp Appl Acarol 52:275–290PubMedCrossRefGoogle Scholar
  41. Martinez-Rocha L, Beers EH, Dunley JE (2008) Effect of pesticides on integrated mite management in Washington State. J Entomol Soc B C 105:1–12Google Scholar
  42. McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their roles in biological control. Annu Rev Entomol 42:291–321PubMedCrossRefGoogle Scholar
  43. McMurtry JA, de Moraes GJ, Famah Sourassou N (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320CrossRefGoogle Scholar
  44. Motoyama N, Rock GC, Dauterman WC (1970) Organophosphorus resistance in an apple orchard population of Typhlodromus (Amblyseius) fallacis. J Econ Entomol 63:1439–1442CrossRefGoogle Scholar
  45. Oatman ER (1976) An ecological study of arthropod populations on apple in northeastern Wisconsin: phytoseiid mite species on the foliage. Environ Entomol 5:63–64CrossRefGoogle Scholar
  46. Pina T, Argolo PS, Urbaneja A, Jacas J (2012) Effect of pollen quality on the efficacy of two different life-style predatory mites against Tetranychus urticae in citrus. Biol Control 61:176–183CrossRefGoogle Scholar
  47. Prischmann DA, James DG, Wright LC, Teneyck RD, Snyder WE (2005) Effects of chlorpyrifos and sulfur on spider mites (Acari: Tetranychidae) and their natural enemies. Biol Control 33:324–334CrossRefGoogle Scholar
  48. Putman WL (1962) Life-history and behaviour of the predacious mite Typhlodromus (T.) caudiglans Schuster (Acarina: Phytoseiidae) in Ontario, with notes on the prey of related species. Can Entomol 94:163–177CrossRefGoogle Scholar
  49. Rhodes EM, Liburd OE, Kelts C, Rondon SI, Francis RR (2006) Comparison of single and combination treatments of Phytoseiulus persimilis, Neoseiulus californicus, and Acramite (bifenazate) for control of twospotted spider mites in strawberries. Exp Appl Acarol 39:213–225PubMedCrossRefGoogle Scholar
  50. SAS Institute (2014a) JMP 11.0. Cary, NCGoogle Scholar
  51. SAS Institute (2014b) SAS/Stat User’s Guide. SAS Institute, Cary, NCGoogle Scholar
  52. Schausberger P, Walzer A (2001) Combined versus single species release of predaceous mites: Predator–predator interactions and pest suppression. Biol Control 20:269–278CrossRefGoogle Scholar
  53. Schmidt RA (2014) Leaf structures affect predatory mites (Acari: Phytoseiidae) and biological control: a review. Exp Appl Acarol 62:1–17PubMedCrossRefGoogle Scholar
  54. Stavrinides MC, Lara JR, Mills NJ (2010) Comparative influence of temperature on development and biological control of two common vineyard pests (Acari: Tetranychidae). Biol Control 55:126–131CrossRefGoogle Scholar
  55. Straub CS, Finke DL, Snyder WE (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol Control 45:225–237CrossRefGoogle Scholar
  56. Strickler K, Cushing N, Whalon M, Croft BA (1987) Mite (Acari) species composition in Michigan apple orchards. Environ Entomol 16:30–36CrossRefGoogle Scholar
  57. Takahashi M, Inoue M, Takafuji A (1998) Management of the spider-mite population in a vinylhouse vinery by releasing Phytoseiulus persimilis Athias-Henriot onto the ground cover. Jpn J Appl Entomol Zool 42:71–76CrossRefGoogle Scholar
  58. Tanigoshi LK, Hoyt SC, Croft BA (1983) Basic biology and management components for mite pests and their natural enemies. In: Croft BA, Hoyt SC (eds) Integrated management of insect pests of pome and stone fruits. Wiley, New York, pp 153–218Google Scholar
  59. Thistlewood H (1991) A survey of predatory mites in Ontario apple orchards with diverse pesticide programmes. Can Entomol 123:1163–1174CrossRefGoogle Scholar
  60. US Department of Agriculture (2015) National Agriculture Statistics Service Spatial Analysis Research Section. Cropland Data Layer. Available: http://www.nass.usda.gov/research/Cropland/SARS1a.htm
  61. Villanueva RT, Harmsen R (1998). Studies on the role of the stigmaeid predator Zetzellia mali in the acarine system of apple foliage. In: Harmsen R (ed) Proceedings, Entomological Society of Ontario, Sudbury, Ontario. Entomological Society of Ontario, pp 149–155Google Scholar
  62. Villanueva R, Walgenbach JF (2005) Development, oviposition, and mortality of Neoseiulus fallacis (Acari: Phytoseiidae) in response to reduced-risk insecticides. J Econ Entomol 98:2114–2120PubMedCrossRefGoogle Scholar
  63. Waite GK (1988) Integrated control of Tetranychus urticae in strawberries in south-east Queensland. Exp Appl Acarol 5:23–32CrossRefGoogle Scholar
  64. Walter DE, Proctor HC (2004) Mites on plants. In: Mites: ecology, evolution, and behaviour. CABI Publishing, Wallingford, pp 169–197Google Scholar
  65. Wearing CH, Marshall RR, Colhoun C, Attfield BA (2014) Phytophagous mites and their predators during the establishment of apple orchards under biological and integrated fruit production in Central Otago, New Zealand. N Z J Crop Hortic Sci 42:127–144CrossRefGoogle Scholar
  66. Whalon M, Korson P (2008) Tart cherry azinphos-methyl transition strategy. A report to the U.S. Environmental Protection Agency. http://epa.gov/pesticides/ppdc/azm/trans-strategy08.pdf

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Rebecca A. Schmidt-Jeffris
    • 1
  • Elizabeth H. Beers
    • 1
  • David W. Crowder
    • 2
  1. 1.Tree Fruit Research and Extension CenterWashington State UniversityWenatcheeUSA
  2. 2.Department of EntomologyWashington State UniversityPullmanUSA

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